Summary
The upper and middle pons and the lower mesencephalon of the cat were explored with extracellular microelectrodes in a search for respiratory related units (RRU). The preparation used, the unanesthetized normocapnic cat, resulted in an “isolated respiratory center” by eliminating input from, as well as output to, lung and thorax. Observations were done in standard experimental conditions which allowed quantitative comparisons of anatomical structures with respect to RRU density (RRUD), RRUD to total unit density (UD) ratio, and a respiratory modulation index (RMI).
Units were recorded in 22 anatomical structures; of 3614 units kept for analysis, 46.9% had a definite respiratory rhythm. The phase relations of frequency variation ere classified into five main categories: 1) tonic expiratory (E) or 2) inspiratory (I) patterns, 3) phase spanning inspiratory-expiratory (IE) or 4) expiratoryinspiratory (EI) patterns, and 5) tonic early expiratory depressed (EED) pattern.
Densely packed RRU were recorded in anatomical structures known to be involved in the command of respiratory accessory musculature (trigeminal system) or thought to be part of the pneumotaxic machinery (nucleus parabrachialis median's, Kölliker-Fuse nucleus). In these structures, RRU proportion was 57–89% of the total neuronal activity.
On the other hand, definite RRU (10–26%) were recorded in structures which are not thought to have a respiratory function (such as inferior colliculus or griseum centralis) where isolate RRU were scattered among non-respiratory tonic units. This group includes nuclei sometimes considered as having a pneumotaxic function.
The pontine reticular formation represents an intermediate category (RRU = 35.6%) where clusters of RRU alternate with non-respiratory modulated cells. The possible role of these clusters is discussed in relation to the hypothesis of multiple coupled respiratory oscillators.
Variance analysis of RRUD, RRUD to UD ratio and RMI shows highly significant differences between the three preceding categories of structures.
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References
Andersen, P., Andersson, S.A.: Physiological basis of the alpha rhythm. 235 pp. New York: Appleton-Century-Crofts 1968.
Baxter, D.W., Olszewski, J.: Respiratory responses evoked by electrical stimulation of pons and mesencephalon. J. Neurophysiol. 18, 276–287 (1955).
Berman, A.L.: The brain stem of the cat. A cytoarchitectonic atlas with stereotaxic coordinates. 175 pp. Madison: The University of Wisconsin Press 1968.
Bertrand, F., Hugelin, A.: Respiratory synchronizing function of nucleus parabrachialis medialis: pneumotaxic mechanisms. J. Neurophysiol. 34, 189–207 (1971).
Blair, E.A., King, C.E., Garrey, W.E.: Inspiratory irradiation. Amer. J. Physiol. 90, 287–288 (1929).
Brookhart, J.M.: The respiratory effects of localized faradic stimulation of the medulla oblongata. Amer. J. Physiol. 129, 709–723 (1940).
Buchsbaum, M., Callaway, E.: Influences of respiratory cycle on simple reaction time. Percept. motor skills 20, 961–966 (1965).
Callaway, E., Buchsbaum, M.: Effects of cardiac and respiratory cycles on averaged visual evoked responses. Electroenceph. clin. Neurophysiol. 19, 476–480 (1965).
Carregal, E.J.A., Williams, B., Birzis, U.: Respiratory centers in the dog and squirrel monkey: a comparative study. Resp. Physiol. 3, 333–348 (1967).
Castaldi, L.: Studi sulla struttura e sullo sviluppo del mesencefalo: Ricerche in cavia cobaya. Parte 3. Arch. ital. Anat. Embriol. 23, 481–609 (1926).
Chapot, G., Hugelin, A., Verroust, J.: Influences des centres respiratoires et de PACO2 sur les réflexes masticateurs. J. Physiol. (Paris) 55, 225 (1963).
Cohen, M.I.: Intrinsic periodicity of the pontile pneumotaxic mechanism. Amer. J. Physiol. 195, 23–27 (1958).
—: Discharge patterns of brain-stem respiratory neurons in relation to carbon dioxide tension. J. Neurophysiol. 31, 142–165 (1968).
—, Hugelin, A.: Suprapontine reticular control of intrinsic respiratory mechanisms. Arch. ital. Biol. 103, 317–334 (1965).
—, Wang, S.C.: Respiratory neuronal activity in pons of cat. J. Neurophysiol. 22, 33–50 (1959).
Costa, J., Chansou, F., Hugelin, A.: Reconnaissance et tri en temps réel des décharges neuroniques unitaires dans un enregistrement multiunitaire. In: “Applications au domaine biomédical des méthodes et technologies de l'électronique”, pp. 70–74. Grenoble: Laboratoire d'électronique et de technologie de l'informatique 1971.
Fuse, G.: Die Randgebiete des Pons und des Mittelhirns. Arb. hirnanat. Inst. Zürich 7, 211–253 (1913).
Gesell, R.: A neurophysiological interpretation of the respiratory act. Ergebn. Physiol. 43, 481–639 (1940).
—, Bricker, J., Magee, C.: Structural and functional organization of the central mechanism controlling breathing. Amer. J. Physiol. 117, 432–452 (1936).
Gootman, P.M., Cohen, M.I.: Efferent splanchnic activity and systemic arterial pressure. Amer. J. Physiol. 219, 897–903 (1970).
Hukuhara, T., Jr., Saji, Y., Kumadaki, N., Kojima, H., Tamaki, H., Takeda, R., Sakai, F.: Die Lokalisation von Atemsynchron entladenden Neuronen in der retikulären Formation des Hirnstammes der Katze unter verschiedenen experimentellen Bedingungen. Arch. exp. Pathol. Pharmakol. 263, 462–484 (1969).
Hugelin, A., Cohen, M.L: The reticular activating system and respiratory regulation in the cat. Ann. N.Y. Acad. Sci. 109, 586–603 (1963).
Jacklet, J.W., Geromino, J.: Circadian rhythms: population of interacting neurons. Science 174, 299–302 (1971).
Johnson, F.H., Russell, G.V.: The locus coeruleus as a pneumotaxic center. Anat. Rec. 112, 348 (1952).
Kahn, N., Wang, S.C.: Electrophysiologic basis for pontine apneustic center and its role in integration of the Hering-Breuer reflex. J. Neurophysiol. 30, 301–318 (1967).
King, C.E.: The effect of respiration on the scratch reflex. Amer. J. Physiol. 98, 368–372 (1931).
—, Blair, E.A., Garey, W.E.: The inspiratory augmentation of proprioceptive reflexes. A study of the knee jerk and the Achilles reflex. Amer. J. Physiol. 97, 329–342 (1931).
Kling, U., Szekely, G.: Simulation of rhythmic nervous activities. I. Function of networks with cyclic inhibitions. Kybernetik 5, 89–103 (1968).
Koepchen, H.P., Seller, H., Polster, J., Langhorst, P.: Über die Fein-Motorik der Muskelstrombahn und ihre Beziehung zur Ateminnervation. Pflügers Arch. 302, 285–299 (1968).
Kölliker, A.: Handbuch der Gewebelehre des Menschen. 6. Aufl. 2. Bd.: Nervensystem des Menschen und der Thiere. 874 pp. Leipzig: Engelmann 1896.
Magne, H.: Recherches sur le mécanisme du frisson thermique et ses relations avec la fonction respiratoire. J. Physiol. (Paris) 18, 527–533 (1919–1920).
Maynard, D.M.: Integration in crustacean ganglia. Symp. Soc. exp. Biol. 20, 111–149 (1966).
Ngai, S.H., Wang, S.C.: Organization of central respiratory mechanisms in the brain stem of the cat: localization by stimulation and destruction. Amer. J. Physiol. 190, 343–349 (1957).
Pavlidis, T.: Populations of interacting oscillators and circadian rhythms. J. theor. Biol. 22, 418–436 (1969).
Richet, C.: Le frisson comme appareil de régulation thermique. Arch. Physiol. 5, 312–326 1893).
St. John, W.M., Glasser, R.L., King, R.A.: Apneustic breathing after vagotomy in cats with chronic pneumotaxic center lesions. Resp. Physiol. 12, 239–250 (1971).
Salmoiraghi, G.C.: Functional organization of brain stem respiratory neurons. Ann. N.Y. Acad. Sci. 109, 571–582 (1963).
—, Burns, B.D.: Localization and patterns of discharge of respiratory neurones in brain stem of cat. J. Neurophysiol. 23, 2–13 (1960).
Scheibel, M.E., Scheibel, A.B.: Structural substrates for integrative patterns in the brain stem retioular core. In: “Reticular formation of the brain”, pp. 31–55. Ed. by H.H. Jasper, L.D. Proctor, R.S. Knighton, W.C. Noshay, R.T. Costello. Boston: Little, Brown and Co. 1958.
Schmidt-Vanderheyden, W., Heinich, L., Koepchen, H.P.: Investigations into the fluctuations of proprioceptive reflexes in man. I. Fluctuations of the patellar tendon reflex and their relation to the vegetative rhythms during spontaneous respiration. Pflügers Arch. 317, 56–71 (1970).
—, Koepchen, H.P.: Investigations into the fluctuations of proprioceptive reflexes in man. II. Fluctuations of the patellar tendon reflex and their relation to vegetative rhythms during controlled respiration. Pflügers Arch. 317, 72–83 (1970).
Seller, H., Langhorst, P., Richter, D., Koepchen, H.P.: Über der Abhängigkeit der pressoreceptorischen Hemmung des Sympathicus von der Atemphase und ihre Auswirkung in der Vasomotorik. Pflügers Arch. 302, 300–314 (1968).
Strughold, H.: Beiträge zur Kenntnis der Refraktärphasen der Eigenreflexe beim gesunden Menschen. Z. Biol. 88, 346–362 (1929).
Takagi, K., Nakayama, T.: Respiratory discharge of the pons. Science 128, 1206 (1958).
Wang, S.C., Ngai, S.H.: Respiration coordinating mechanism of the brain stem. A few controversial points. Ann. N.Y. Acad. Sci. 109, 550–559 (1963).
Wilson, D.M.: The central nervous control of flight in a locust. J. exp. Biol. 38, 471–490 (1961).
—: Neural operations in arthropod ganglia. In: “The neurosciences. Second study program”, pp. 397–409. Ed. by F.O. Schmitt. New York: Rockefeller University Press 1970.
—, Wyman, R.J.: Motor output patterns during random and rhythmic stimulation of locust thoracic ganglia. Biophys. J. 5, 121–143 (1965).
Woldring, S., Dirken, M.N.J.: Site and extension of bulbar respiratory center. J. Neurophysiol. 14, 227–241 (1951).
Wright, S.: Applied physiology. Ninth edition. XVI-1190 pp. London: Oxford University Press 1952.
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This work was supported in part by grants from Délégation générale à la Recherche scientifique et technique (6600431) and Centre national de la Recherche scientifique (ERA 233). We thank Dr. M.I. Cohen for his help in the english composition of the manuscript. J. Costa and F. Chansou are gratefully acknowledged for writing the respiratory unit (RSPUNIT) program.
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Bertrand, F., Hugelin, A. & Vibert, J.F. Quantitative study of anatomical distribution of respiration related neurons in the pons. Exp Brain Res 16, 383–399 (1973). https://doi.org/10.1007/BF00233430
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DOI: https://doi.org/10.1007/BF00233430